Skip to main content
Log in

Ectomycorrhizal fungus enhances drought tolerance of Pinus sylvestris var. mongolica seedlings and improves soil condition

  • Original Paper
  • Published:
Journal of Forestry Research Aims and scope Submit manuscript

Abstract

Mongolian pine is an important afforestation species widely used for ecological management in northeast China. The environment in this region is very unstable and the flora are regularly subjected to drought stress. This paper reports on the influence of inoculation with the Suillus luteus on seedlings under different water conditions. Both inoculated and non-inoculated ectomycorrhizal fungi (ECMF)-S. luteus seedlings were maintained under well-watered or water-stress conditions for 3 months. The S. luteus colonization rate under water stress was higher than that in well-watered conditions. Under water stress, inoculated seedlings had greater growth than non-inoculated seedlings. In addition, under water stress, S. luteus-inoculated seedlings had greater superoxide dismutase and peroxidase activity, higher soluble protein content, lower proline content, and lower malondialdehyde content than non-inoculated seedlings. S. luteus colonization increased the rhizosphere soil-enzyme activity and the rhizosphere soil nutrition content under both well-watered and water-stress conditions. Given the positive impact on seedling growth and physiology, S. luteus shows potential for use in the arid and semi-arid regions of northeast China for afforestation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abbaspour H, Saeidi-Sar S, Afshari H, Abdel-Wahhab MA (2012) Tolerance of Mycorrhiza infected Pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. J Plant Physiol 169:704–709

    Article  CAS  Google Scholar 

  • Baar J, Stanton NL (2000) Ectomycorrhizal fungi challenged by saprotrophic basidiomycetes and soil microfungi under different ammonium regimes in vitro. Mycol Res 104:691–697

    Article  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bending GD, Read DJ (1995) The structure and function of the vegetative mycelium of ectomycorrhizal Plants. Vl Activities of nutrient moblizing enzymes in birch litter colonized by Paxillus involutus. N Phytol 130:411–417

    Article  CAS  Google Scholar 

  • Birhane E, Sterck FJ, Fetene M, Bongers F, Kuyper TW (2012) Arbuscular mycorrhizal fungi enhance photosynthesis, water use efficiency, and growth of frankincense seedlings under pulsed water availability conditions. Oecologia 169:895–904

    Article  Google Scholar 

  • Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111

    Article  CAS  Google Scholar 

  • Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N (1996) Working with mycorrhizas in forestry and agriculture. Australian Centre for International Agricultural Research Monograph, Canberra, p 32

    Google Scholar 

  • Cairney JWG, Chambers SM (1999) Ectomycorrhizal fungi-key genera in profile. Springer, Berlin

    Book  Google Scholar 

  • Christos DG, Konstantinos G, George Z (2008) Mechanism of Coomassie brilliant blue G-250 binding to proteins: a hydrophobic assay for nanogram quantities of proteins. Anal Bioanal Chem 391:391–403

    Article  Google Scholar 

  • Edda S, Oddsdottir ES, Eilenberg J, Sen R, Halldorsson G (2010) The effects of insect pathogenic soil fungi and ectomycorrhizal inoculation of birch seedlings on the survival of Otiorhynchus larvae. Agr Entomol 12:319–324

    Google Scholar 

  • Gong MG, Tang M, Chen H, Zhang QM, Feng XX (2013) Effects of two glomus species on the growth and physiological performance of Sophora davidii seedlings under water stress. N For 44:399–408

    Google Scholar 

  • Guang SY (1986) Soil enzyme and research method. Agricultural Press, Beijing, pp 323–328

    Google Scholar 

  • Ho L, Zak B (1979) Acid Phosphatase activity of six ectomycorrhizal Douglas fir rootlets and some mycorrhizal fungi. Plant Soil 54:395–398

    Article  Google Scholar 

  • Huang Y, Jiang XY, Liang ZC, Li T (2006) Effect of ectomy-corrhizal fungi on growth and physiology of Pinus tabulaeformis seedlings under saline stress. J Agro Environ 25(6):1475–1480

    Google Scholar 

  • Huang Z, Zou ZR, He CX, He ZQ, Zhang ZB, Li JM (2011) Physiological and photosynthetic responses of melon (Cucumis melo L.) seedlings to three glomus species under water deficit. Plant Soil 339:391–399

    Article  CAS  Google Scholar 

  • Jaleel CA, Riadh K, Gopi R, Manivannan P, Al-Jaburi HJ, Zhao CX, Shao HB, Panneerselvam R (2009) Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol Plant 31:427–436

    Article  Google Scholar 

  • Karaba A, Dixit S, Greco R, Aharoni A, Trijatmiko KR, Marsch Martinez N, Krishnan A, Nataraja KN, Udayakumar M, Pereira A (2007) Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene. Proc Natl Acad Sci USA 104:15270–15275

    Article  CAS  Google Scholar 

  • Martins A (2004) Micorrizac¸a˜o controlada de Castanea sativa Mill:aspectos fisiolo´gicos da micorrizac¸a˜o in vitro. Tese de Doutoramento, Faculdade de Cieˆncias da Universidade de Lisboa, Lisboa

  • Martins A, Casimiro A, Pais MS (1997) Influence of mycorrhization on physiological parameters of micropropagated Castanea sativa Mill. plants. Mycorrhiza 7:161–165

    Article  CAS  Google Scholar 

  • Miller OKJ (1982) Taxonomy of ecto- and ectendomycorrhizal fungi. Methods Princ Mycorrhizal Res 91–101

  • Mucha J, Dahm H, Strzelczyk E, Werner A (2006) Synthesis of enzymes connected with mycoparasitism by ectomycorrhizal fungi. Arch Microbiol 185:69–77

    Article  CAS  Google Scholar 

  • Nannipieri P, Ceccanti B, Cervelli S, Matarese E (1980) Extraction of phosphatase, urease, protease, organic carbon and nitrogen from soil. Soil Sci Soc Am J 44:1011–1016

    Article  CAS  Google Scholar 

  • Ravi S, Breshears DD, Huxman TE, D’Odorico P (2010) Land degradation in drylands: interactions among hydrologic-aeolian erosion and vegetation dynamics. Geomorphology 116:236–245

    Article  Google Scholar 

  • Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317

    Article  Google Scholar 

  • Sharma R, Rajak RC, Pandey AK (2010) Evidence of antagonistic interactions between rhizosphere and mycorrhizal fungi associated with Dendrocalamus strictus (Bamboo). J Yeast Fungal Res 1:112–117

    Google Scholar 

  • Sharma S, Villamor JG, Verslues PE (2011) Essential role of tissue-specific proline synthesis and catabolism in growth and redox balance at low water potential. Plant Physiol 157:292–304

    Article  CAS  Google Scholar 

  • Shaw TM, Dighton J, Sanders FE (1995) Interactions between ectomycorrhizal and saprotrophic fungi on agar and in association with seedlings of lodgepole pine (Pinus contorta). Mycol Res 99:159–165

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, San Diego

    Google Scholar 

  • Song XS, Hu WH, Mao WH, Ogweno JO, Zhou YH, Yu JQ (2005) Response of ascorbate peroxidase isoenzymes and ascorbate regeneration system to abiotic stresses in Cucumis sativus. Plant Physiol Biochem 43:1082–1088

    Article  CAS  Google Scholar 

  • Tabatabai MA (1982) Soil enzymes. In: Page AL, Miller RH, Keeney (eds) Methods of soil analyses, part 2, chemical and microbiological properties, 2nd edn. American Society of Agronomy, Madison, pp 903–947

    Google Scholar 

  • Thomson BD, Grove TS, Malajczuk N, Hardy GE (1994) The effectiveness of ectomycorrhizal fungi in increasing the growth of Eucalyptus globulus Labill. in relation to root colonization and hyphal development in soil. N Phytol 126:517–524

    Article  Google Scholar 

  • Turjaman M, Tamai Y, Segah H, Limin SH, Cha JY, Osaki M, Tawaraya K (2005) Inoculation with the ectomycorrhizal fungi Pisolithus arhizus and Scleroderma sp. improves early growth of Shorea pinanga nursery seedlings. N For 30:167–173

    Google Scholar 

  • Vinale F, D’Ambrosio G, Abadi K, Scala F, Marra R, Turra D, Woo SL, Lorito M (2004) Application of Trichoderma harzianum (T22) and Trichoderma atroviride (P1) as plant growth promoters, and their compatibility with copper oxychloride. J Z J Univ Sci 30:2–8

    Google Scholar 

  • Wang XM, Chen F, Hasi E, Li JC (2008) Desertification in China: an assessment. Earth Sci Rev 88:188–206

    Article  Google Scholar 

  • Wang RY, Yu SQ, Zhang JC, Zhou CF, Chen LS (2012) Effects of mycorrhizal fungus inoculation on the root of Cupressus duclouxiana and Catalpa bungei seedlings under drought stress. J Nanjing For Univ Nat Sci Edn 36:23–27

    Google Scholar 

  • Wasowicz W, Jean N, Peratz A (1993) Optimized steps in fluorometric determination of thiobarbituric acid reactive substances in serum; importance of extraction pH and influence of sample preservation and storage. Clin Chem 38(12):2522–2526

    Google Scholar 

  • William PI, Paul RB (1985) Extinction coefficients of chlorophyll a and b in N, N-dimethyl formamide and 80% acetone. Plant Physiol 77:483–485

    Article  Google Scholar 

  • Wu QS, Xia RX, Hu ZJ (2006) Effect of arbuscular mycorrhiza on the drought tolerance of Poncrius trifoliata seedlings. Front For China 1:100–104

    Article  Google Scholar 

  • Wu QS, Xia RX, Zou YN (2008) Improved soil structure and citrus growth after inoculation with three arbuscular mycorrhizal fungi under drought stress. Eur J Soil Biol 44:122–128

    Article  Google Scholar 

  • Xu HY, Lei SM, Xiong W (2012) Rhizospheric niche of Carrizo citrange seedlings colonized arbuscular mycorrhizal (AM) fungi. J SW Univ 34(10):65–71

    CAS  Google Scholar 

  • Yang XH, Zhang KB, Jia BQ, Ci LJ (2005) Desertification assessment in China: an overview. J Arid Environ 63:517–531

    Article  Google Scholar 

  • Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514

    Article  CAS  Google Scholar 

  • Yin DC, Deng X, Ilan Chet, Song RQ (2014) Physiological responses of Pinus sylvestris var. Mongolica seedlings to the interaction between Suillus luteus and Trichoderma virens. Curr Microbiol 69:334–342

    Article  CAS  Google Scholar 

  • Yin DC, Qi JY, Deng JF, Du H, Deng X (2017) Effects of Ectomycorrhizal cooperating with exogenous calcium on Pinus sylvestris var. mongolica growth. China Environ Sci 37(6):2295–2304

    Google Scholar 

  • Yooyongwech S, Phaukinsang N, Cha-um S, Supaibulwatana K (2013) Arbuscular mycorrhiza improved growth performance in Macadamia tetraphylla L. grown under water deficit stress involves soluble sugar and proline accumulation. Plant Growth Regul 69:285–293

    Article  CAS  Google Scholar 

  • Zantua MI, Bremner JM (1975) Comparison of methods of assaying urease activity in soils. Soil Biol Biochem 7:91–295

    Google Scholar 

  • Zhang Q (2003) Studies on the cytology of pathogenic mechanism of LA-toxin. Nanjing Forestry University, Nanjing

    Google Scholar 

  • Zhang Y, Zhong CL, Chen Y, Chen Z, Jiang QB, Wu C, Pinyopusarerk K (2010) Improving drought tolerance of Causarina equisetifolia seedlings by arbuscular mycorrhizas under glasshouse conditions. N For 40:261–271

    Google Scholar 

  • Zhang RQ, Tang M, Chen H, Tian ZQ (2011) Effects of ectomycorrhizal fungi on damping-off and induction of pathogenesis-related proteins in Pinus tabulaeformis seedlings inoculated with Amanita vaginata. For Pathol 41:262–269

    Article  Google Scholar 

  • Zhang ZF, Zhang JC, Huang YQ (2014) Effects of arbuscular mycorrhizal fungi on the droughttolerance of Cyclobalanopsis glauca seedlings under greenhouse conditions. N For 45:545–556

    CAS  Google Scholar 

  • Zheng X, Zhu JJ, Yan QL, Song LN (2012) Effects of land use changes on the groundwater table and the decline of Pinus sylvestris var. mongolica plantations in southern Horqin Sandy Land, Northeast China. Agric Water Manag 109:94–106

    Article  Google Scholar 

  • Zhu XC, Song FB, Xu HW (2010) Influence of arbuscular mycorrhiza on lipid peroxidation and antioxidant enzyme activity of maize plants under temperature stress. Mycorrhiza 20:325–332

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ruiqing Song.

Additional information

Project funding: The work was supported by the National Natural Science Foundation of China (31670649, 31200484, 31170597).

The online version is available at http://www.springerlink.com

Corresponding editor: Tao Xu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yin, D., Song, R., Qi, J. et al. Ectomycorrhizal fungus enhances drought tolerance of Pinus sylvestris var. mongolica seedlings and improves soil condition. J. For. Res. 29, 1775–1788 (2018). https://doi.org/10.1007/s11676-017-0583-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11676-017-0583-4

Keywords

Navigation